METAMORPHOSIS A Problem in Developmental Biology

2ND EDmON

METAMORPHOSIS A Problem in Developmental Biology

2ND EDmON

Edited by LAWRENCE I. GILBERT The University of North Carolina Chapel Hill, North Carolina

and EARL FRIEDEN Florida State University Tallahassee, Florida

PLENUM PRESS · NEW YORK AND LONDON

Library of Congress Cataloging in Publication Data

Main entry under title:

Metamorphosis, a problem in developmental biology.

Includes bibliographies and index. 1. Metamorphosis. I. Gilbert, Lawrence Irwin, 1929-

[DNLM: 1. Metamorphosis, Biological. QL 981 M587] II. Frieden, Earl.

QL981.M47 1981 591.3'34

ISBN-13: 978-1-4613-3248-0 DOl: 10.1007/978-1-4613-3246-6

© 1981 Plenum Press, New York

e-ISBN: 978-1-4613-3246-6

Softcover reprint of the hardcover 1 st edition 1981 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013

All rights reserved

81-17691 AACR2

No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the publisher

Contributors

Burr G. Atkinson, Department of Zoology, Cell Science Laboratories, University of Western Ontario, London, Ontario, Canada

Walter E. Bollenbacher, Department of Anatomy and Department of Zo­ology, University of North Carolina, Chapel Hill, North Carolina 27514

Robert H. Broyles, Department of Biochemistry and Molecular Biology, University of Oklahoma at Oklahoma City, Health Sciences Center, Oklahoma City, Oklahoma 73190

Virginia Carver, Department of Chemistry, The Florida State University, Tallahassee, Florida 32306

Ernest S. Chang, Department of Animal Science, University of California, Davis, California 95616, and Bodega Marine Laboratory, P.O. Box 247, Bodega Bay, California 94923

Deborah Ann Check, Physiology Group, T. H. Morgan School of Biolog­ical Sciences, University of Kentucky, Lexington, Kentucky 40506

Harold Fox, Department of Zoology, University College, London WC1E 6BT, United Kingdom

Earl Frieden, Department of Chemistry, Florida State University, Talla­hassee, Florida 32306

James W. Fristrom, Department of Genetics, University of California, Berkeley, California 94720

Lawrence I. Gilbert, Department of Zoology4 University of North Car­. olina, Chapel Hill, North Carolina 27514

Walter Goodman, Department of Entomology, University of Wisconsin, Madison, Wisconsin 53706

Noelle A. Granger, Department of Anatomy and Department of Zoology, University of North Carolina, Chapel Hill, North Carolina 27514

K. C. Highnam, Department of Zoology, The University, Sheffield SlO 2TN, United Kingdom

John J. Just, Physiology Group, T. H. Morgan School of Biological Sci­ences, University of Kentucky, Lexington, Kentucky 40506

Jerry J. Kollros, Department of Zoology, University of Iowa, Iowa City, Iowa 52242

Jeanne Kraus-Just, Physiology Group, T. H. Morgan School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506

v

vi CONTRIBUTORS

M. Locke, The Cell Science Laboratories, Zoology Department, Univer­sity of Western Ontario N6A 5B7, Canada

Charles S. Nicoll, Department of Physiology-Anatomy, University of California, Berkeley, California 94720

John D. O'Connor, Department of Biology, University of California, Los Angeles, California 90024

Sandra J. Smith-Gill, Department of Zoology, University of Maryland, College Park, Maryland 20742

S. Sridhara, Department of Biochemistry, University of Mississippi Med­ical Center, Jackson, Mississippi 39216

George Wald, Biological Laboratories of Harvard University, Cambridge, Massachusetts 02138

Bruce A. White, Department of Physiology-Anatomy, University of Cal­ifornia, Berkeley, California 94720. Present address: Laboratory of Cellular Gene Expression and Regulation, Memorial Sloan-Kettering Cancer Center, New York, New York 10021

A Personal Foreword

"The old order changeth, yielding place to new." When Tennyson wrote this, he was unfamiliar with the pace of modem science else he would have said the new is displaced by the newer. When Gilbert and I gathered the papers for the first edition of this overview of metamorphosis, we aimed to provide a broad basis upon which the experimental analysis of the developmental changes called metamorphosis could proceed. We were both aware then that with the new techniques of biochemistry and with the revolutionary breakthrough to the nature of the gene, countless new possibilities were being opened for the exploration of the molecular basis of development. The resources offered by metamorphic changes offered unique opportunities to trace the path from gene to phenotype. Our expectations were high. I visited Larry Gilbert and Earl Frieden in their laboratories and saw with envy how far advanced they were then in the use of molecular methods of analysis. I had started on a different approach to develop an in vitro test for thyroid action on amphibian tissue. But circumstances limited my own progress to the initial delim­itation of the technical possibilities of the in vitro system. Only from the sidelines could I watch the steady if slow progress of biology in penetrating the maze of molecular events by which animal tissues re­spond to hormonal and other developmental factors. In retirement, I succumbed to the inevitable and turned to an old love-social behavior and the new speculations of sociobiology. Hence, I now look forward as a novice in a strange land to reading this new text. However, unlike Sir Bedivere, who was reluctant to throw the sword Excalibur into the lake, we in science think that a thirteen-year-old review of so rich a topic as metamorphosis has waited, perhaps too long, to be displaced by the new. I congratulate Larry and Earl on the splendid talents they have persuaded to contribute to this new edition and, unlike Sir Bedivere, I look forward to a new Camelot.

WILLIAM ETKIN

vii

Preface

Amphibian and insect metamorphosis has excited the interest and imag­ination of man since the time of Aristotle. Metamorphosis exemplifies the most profound change in form found during the postembryonic de­velopment of all animals. As early as the late 1800s the process was recognized as reflecting significant steps in biological evolution both vertebrate and invertebrate. More recently a wide spectrum of life sci­entists ranging from developmental biologists to biochemists have ad­dressed the fundamental questions related to metamorphosis. The com­manding role of both invertebrate and vertebrate hormones was quickly recognized and exploited by endocrinologists and other biologists. Cur­rently, molecular biologists-who were formerly preoccupied with phage and Escherichia coli-have begun to focus their attention on the prob­lems of cellular transitions and to utilize animal forms that undergo metamorphosis as a model system for the study of development and differentiation.

The presence of several authoritative reviews on specific facets of this subject does not mitigate the need for a thorough and systematic work that brings together the many disparate strands of knowledge and research on metamorphosis. This work presents in a single volume the numerous aspects of metamorphosis, as did the first volume of Met­amorphosis: A Problem in Developmental Biology, published in 196-8. Except for the title and subject matter, there is a minimum of overlap between the two editions. The subject has been arranged to permit several points of view. A new group of contributors has been encouraged to use their own unique approaches and styles to keep the volume diverse and stimulating.

The book has been designed primarily for research scientists and biology graduate students. It should be useful in any college course en­compassing development, endocrinology, physiology, or biochemistry. We recommend it for scholars interested in growth and development, from undergraduate juniors to senior researchers.

Tallahassee, Florida Chapel Hill, North Carolina

ix

Earl Frieden Lawrence I. Gilbert

Contents

Chapter 1

Metamorphosis: An Overview George Wald

1. Introduction ................................................................................. 1 2. Primacy of the Spawning Environment ..................................... 8 3. Internal or External Salinity-Which Determines the Visual

Pattern? ......................................................................................... 14 4. Euryhaline Fishes and Amphibians ............................................ 16 5. Biochemistry of Metamorphosis ................................................. 19 6. Second Metamorphosis ................................................................ 23 7. Deep-Sea Fishes; Eels .................................................................. 28 8. Land Vertebrates .......................................................................... 32 9. Conclusion ................................................................................... 36

10. Epilogue ........................................................................... ,'............ 36 References ........................................................................................... 38

PART I: INSECTS

Chapter 2

A Survey of Invertebrate Metamorphosis K. C. Highnam

1. Introduction ................................................................................. 43 2. Invertebrate Metamorphoses ... ............ .............. ....... ......... .......... 45

2.1. Porifera ............................................................................... 46 2.2. Cnidaria.............................................................................. 46

xi

xii CONTENTS

2.3. Ctenophora ......................................................................... 47 2.4. Platyhelminthes ................................................................. 47 2.5. Nemertinea ........................................................................ 50 2.6. Acanthocephala............................................................. ..... 51 2.7. Aschelminthes ................................................................... 52 2.8. Rotifera ............................................................................... 52 2.9. Kinorhyncha ....................................................................... 52 2.10. Priapulida ........................................................................... 53 2.11. Entoprocta ............. ........ ..................................................... 53 2.12. Polyzoa ............................................................................... 53 2.13. Brachiopoda ........................................................................ 54 2.14. Annelida ............................................................................. 54 2.15. Sipunculida ......................................................................... 55 2.16. Echiurida .... ,....................................................................... 56 2.17. Arthropoda ......................................................................... 56 2.18. Mollusca ............................................................................. 58 2.19. Echinodermata ................................................................... 60 2.20. Phoronidea ............................................... ........................... 62 2.21. Chaetognatha ..................................................................... 63 2.22. Hemichordata ................................. .................................... 63

3. Comparison of Insect Metamorphosis with That of Other Invertebrates ................................................................................. 63 3.l. Ametabolous Development ............................................... 64 3.2. Hemimetabolous Development ........................................ 64 3.3. Holometabolous Development ......................................... 65 3.4. Hypermetamorphosis ......................................................... 67

4. Control of Metamorphosis .......................................................... 68 4.l. Larval Settlement and Metamorphosis ............................ 68 4.2. The Timing of Metamorphosis ........................................ ; 70

5. Conclusions .................................................................................. 71 References ........................................................................................... 72

Chapter 3

Cell Structure during Insect Metamorphosis

M. Locke

1. Introduction ................................................................................. 75 l.l. The Nature of Metamorphosis ......................................... 75 l.2. Definition of Terms ........................................................... 76

2. Tissue Reorganization ................................................................. 78 2.1. Metamorphic Changes in the Arrangement of Cells in

Lepidopteran Fat Body ....................................................... 78 2.2. Changes in the Location of Cells-Epidermal and Muscle

Rearrangement ................................................................... 80

CONTENTS xiii

2.3. Changes in Composition and the Distribution of Reserves .............................................................................. 81

3. Cell Remodeling .......................................................................... 83 3.1. The General Mechanism of Autophagy........................... 84 3.2. Repopulation with New Organelles ................................. 86 3.3. Membrane Changes and Membrane Turnover ................ 87 3.4. The Cytoskelton and Changes in Shape and Organelle

Distribution ...... .............................. ........ ............................ 90 3.5. Cell Coupling and Junctions ............................................. 91 3.6. The Control of Remodeling .............................................. 91

4. Changes in the Numbers and Kinds of Cells in Remodeling to Make New Tissues ...................................................................... 92 4.1. Cell Division ...................................................................... 93 4.2. Cell Death .......................................................................... 93 4.3. Polyploidy and Polyteny .................................................... 95

5. The Morphology Needed to Explain Some Aspects of Metamorphosis ............................................................................. 96 5.1. Hormonal Signals and the Response of the Nucleus ...... 96 5.2. Positional Signals and the Kind and Amount of Growth 97 5.3. The Reception and Use of Nutritional and Precursor

Molecules: Pinocytosis and Transepithelial Transport ... 100 6. Discussion .................................................................................... 100

6.1. The Onset of Metamorphosis ........................................... 100 6.2. Comparisons between Insects and Vertebrates ............... 101

References ........................................................................................... 101

Chapter 4

Hormonal Control of Insect Metamorphosis Noelle A. Granger and Walter E. Bollenbacher

1. Introduction ................................................................................. 105 2. Classical Methods for the Study of the Endocrinology of Insect

Metamorphosis ............................................................................. 107 3. The Insect Endocrine System: Structural Components of the

Classical Scheme ......................................................................... 108 3.1. The Brain-Neurosecretory Cells .................................... 108 3.2. Neurohemal Organs .......................................................... 110 3.3. Prothoracic Glands ............................................................ III 3.4. Corpora Allata .................................................................... III

4. Studies Leading to the Elaboration of the Classical Scheme .... 112 5. Chemistry and Endocrinology of the Metamorphic Hormones 115

5.1. Brain Hormone ................................................................... 115 5.2. Molting Hormones (Ecdysteroids) ..................................... 119 5.3. Juvenile Hormones ............................................................ 121

xiv CONTENTS

6. Control of Endocrine Glands ...................................................... 124 6.1. Cerebral NSC ..................................................................... 124 6.2. The PG ............................................................................... 127 6.3. The CA ................................................................................ 130

7. Summary ...................................................................................... 134 References ... ... ...... ...... ... ........ ..... ........ ... ....... ..... ....... ... ............. ..... ...... 136

Chapter 5 Chemistry, Metabolism, and Transport of Hormones Controlling Insect Metamorphosis Lawrence 1. Gilbert and Walter Goodman

1. Introduction ....... ..... .............. ... ......... ... ..... .............. ....... ....... ....... 139 2. Prothoracicotropic Hormone ....................................................... 140 3. Molting Hormone ......... ; .............................................................. 142

3.1. Ecdysteroids-Chemistry and Occurrence ...................... 142 3.2. Biosynthesis of Ecdysone and 20-Hydroxyecdysone ........ 145 3.3. Ecdysteroid Transport ........................................................ ISS 3.4. Ecdysteroid Degradation .................................................... 156

4. Juvenile Hormones ...................................................................... 158 4.1. Chemistry and Occurrence ............................................... 158 4.2. Structure-Activity Relationships ..................................... 159 4.3. Transport ............................................................................ 161 4.4. Biosynthesis ....................................................................... 168 4.5. Degradation ...... ........ ...... .......... ... ....... ... ........... ... .......... ..... 170

References ........................................................................................... 173

Chapter 6 Macromolecular Changes during Insect Metamorphosis

S. Sridhara

1. Introduction .. ...... .... ... ..... ...... .......... ... ..... .......... ............ ... ....... ..... 177 2. Changes in Protein and RNA during Larval-Pupal-Adult

Metamorphosis ............................................................................. 179 2.1. Breakdown of Macromolecular Components ................... 181 2.2. Synthesis of Macromolecular Components ..................... 185 2.3. Cuticular Proteins ............................................................. 192

3. Pupal-Adult Metamorphosis: Wing Development .................... 193 4. Larval-Pupal Metamorphosis ...................................................... 204

4.1. Epidermis.. ....... ..... ... ... .......... ... ..... ... ....... ... ....... ........ ... ....... 204 4.2. Fat Body.. ... ...... ... ... ........ ... ..... ........ ..... ....... ... ....... ........ ... .... 208

CONTENTS xv

5. Conclusions .................................................................................. 214 References ........................................................................................... 215

Chapter 7

Drosophila Imaginal Discs as a Model System for the Study of Metamorphosis

James W. Fristrom

1. Introduction and Background ...................................................... 217 1.1 General Characteristics of Mass-Isolated Imaginal Discs 218

2. Characteristics of Disc Metamorphosis ..................................... 219 2.1. Late-Larval and Prepupal Development ........................... 219 2.2. Specificity of Ecdysteroid Induction of Disc

Metamorphosis .................................................................. 220 2.3. Ecdysteroid Receptors in Imaginal Discs ......................... 222 2.4. Effects of Ecdysteroids on Discs ....................................... 231

3. Discussion .................................................................................... 236 3.l. Direct Nuclear Action of Hormones ................................ 237 .3.2. Instability of Hormone-Receptor Complex ..................... 237 3.3. Multiplicity of Target Tissues .......................................... 238 3.4. Evolutionary Origin of Metamorphic Hormone

Responsiveness .................................................................. 238 References ............................................................ ,.............................. 240

Chapter 8

Cell Lines as a Model for the Study of Metamorphosis

John D. O'Connor and Ernest S. Chang

1. Introduction ................................................................................. 241 1.1. Advantages of Cell Lines ................................................... 241 1.2. Cell Types Present in Established Cell Lines .................. 243

2. Responses of Established Cell Lines to Ecdysteroids ................ 244 2.1. Morphological Alterations ................................................ 244 2.2. Enzyme Induction .............................................................. 249 2.3. Cell-Surface Changes ......................................................... 250 2.4. Cell-Cycle Changes ........................................................... 250 2.5. Ecdysteroid Receptors ........................................................ 251

3. Responses of Established Cell Lines to Juvenile Hormones ..... 253 3.1. Proliferation and Morphological Effects ........................... 253 3.2. Macromolecular Synthesis ........... ................ ..................... 255 3.3. Juvenile Hormone Metabolism ......................................... 255 3.4. Juvenile Hormone Receptors ............................................ 257

4. Conclusions .................................................................................. 259 References ........................................................................................... 260

xvi CONTENTS

PART II: VERTEBRATES

Chapter 9

Survey of Chordate Metamorphosis John J. Just, Jeanne Kraus-Just, and Deborah Ann Check

1. Introduction ........ ...... .................................................... ........ ....... 265 2. Urochordates . ................................ ...... ......................................... 269

2.1. Appendicularia ................................................................... 269 2.2. Thaliacea ............................................................................ 270 2.3. Ascidians ............................................................................ 271 2.4. Triggers of Metamorphic Climax ........ ........ .......... ........... 274 2.5. Unresolved Questions in Urochordate Metamorphosis .. 276

3. Cephalochordates ......................................................................... 277 3.1. Cephalochordate Feeding Behavior ................................... 280 3.2. Triggers for Metamorphosis .............................................. 282 3.3. Unresolved Questions in Cephalochordate

Metamorphosis .................................................................. 282 4. Fish ............................................................................................... 283

4.1. Agnatha .............................................................................. 283 4.2. Chondrichthyes.................................................................. 291 4.3. Osteichthyes ...................................................................... 292

5. Amphibians .................................................................................. 299 5.1. Parental Care ...................................................................... 300 5.2. Larval Morphology and Staging ........................................ 302 5.3. Larval Life Span and Survival Rates ................................. 311 5.4. Amphibian Larval Behavior .............................................. 313 5.5. Triggers for Amphibian Metamorphosis .......................... 318 5.6. Problem Areas in Amphibian Metamorphosis ................. 319

6. Future Work in Chordate Metamorphosis ................................. 320 References ........................................................................................... 321

Chapter 10

Cytological and Morphological Changes during Amphibian Metamorphosis Harbld Fox

1. Introduction .......................... ........ .......................... ........... .......... 327 2. The Thyroid . .......... .................... ........................... ....................... 328 3. The Central Nervous System and Associated Notochord ........ 330

3.1. General Development of the CNS ........ .......... ........ .......... 330 3.2. The Mauthner Cells .......... ........ ........ .................. ...... ........ 330

CONTENTS xvii

3.3. Lateral Motor Column Cells ............................................. 331 3.4. Fine Structure of LMC Cells and Their Degeneration .... 332 3,5. Tail Nerve Cord ................................................................. 334 3.6. General Structure and Development of the Notochord .. 335 3.7. Notochordal Fine Structure and Its Degeneration .......... 335

4. The Alimentary Canal...... .......... ............ .............. .............. ......... 336 5. The Pancreas ................................................................................ 341 6. The Liver ........................................................................... ........... 343 7. The Pronephros ............................................................................ 346

7.1. Structure and Development .............................................. 346 7.2. Fine Structure .................................................................... 348 7.3. Degeneration ...................................................................... 349

8. The Skin ....................................................................................... 352 8.1. Early Epidermal Cellular Differentiation ......................... 353 8.2. General Structure of Larval Skin ...................................... 354 8.3. Degeneration of Larval Tail and Body Skin ..................... 356 8.4. Thyroid Hormones and Larval Skin ................................. 358

References ........................................................................................... 361

Chapter 11 Hormonal Control of Amphibian Metamorphosis Bruce A. White and Charles S. Nicoll

1. Introduction ............................................................... .................. 363 2. The Thyroid ................................................................................. 364

2.1. Thyroid Function during Premetamorphosis ...... ............. 364 2.2. Thyroid Function during Prometamorphosis and

Climax ............................................................................... 366 2.3. Thyroid Function in Larval Urodeles ............................... 371 2.4. Metabolism of Thyroid Hormones .. ................ ............ ..... 372 2.5. Tissue Sensitivity to T3 and T4 ........................................ 373 2.6. Pituitary Regulation of Thyroid Function .. .............. ....... 374 2.7. Control of Thyrotropic Function by Thyroid Hormones 376 2.8. Control of Thyrotropic Function by the Brain ................ 376 2.9. Effects of Thyroid Hormones on Hypothalamo-

Hypophysial Development and Function ............ ............. 378 3. Prolactin ....................................................................................... 380

3.1. PRL, GH, and Growth ....................................................... 380 3.2. Antimetamorphic Actions of PRL .................................... 383 3.3. PRL-Thyroid Interactions in "Second Metamorphosis" 385 3.4. Control of PRL Secretion and PRL Levels during

Metamorphosis .................................................................. 386 4. Adrenocortical Hormones ........................................................... 387 5. Osmoregulation and Metamorphosis ......................................... 389

xviii CONTENTS

6. Control of Anuran Development and Activation of Metamorphic Climax .................................................................. 391

7. Conclusions .................................................................................. 393 References .......... ............ ........ ........ ............ .......... ............ .... ............... 394

Chapter 12

Biological Basis of Tissue Regression and Synthesis Burr G. Atkinson

1. Introduction ................................................................................. 397 2. Spontaneous and Thyroid-Hormone-Induced Differentiation

and Development of Anuran Tadpole Limbs and Lungs ... ........ 398 2.1. Introduction ... ........ ........ .......... ............ ................ ..... ......... 398 2.2. Tadpole Limbs . ........ ...... ............ .......... ....... ........... ..... ....... 398 2.3. Tadpole Lungs .................................................................... 412 2.4. Conclusion ......................................................................... 415

3. Spontaneous and Thyroid-Hormone-Induced Degeneration of Anuran Tadpole Tail and Gills ................................................... 415 3.1. Introduction ....................................................................... 415 3.2. Tadpole Tail ....................................................................... 416 3.3. Tadpole Gills ........ ........ .......... .......... ................ ..... ....... ...... 437 3.4. Conclusion: Model for Hormone-Modulated

Degeneration ...................................................................... 443 References ........................................................................................... 443

Chapter 13 Transitions in the Nervous System during Amphibian Metamorphosis Jerry J. Kollros

1. Introduction ................................................................................. 445 2. Gross Changes ............................................................................. 445 3. Mesencephalic Fifth Nucleus ...................................................... 446 4. Mauthner's Neuron ..................................................................... 448 5. Lateral Motor Column .. .......... ............ .......... ............ ............ ...... 449 6. Dorsal Root Ganglia ..................................................................... 451 7. Rohon-Beard Cells ...................................................................... 452 8. Cerebellum . ...... ........ ...... .......... .......... ...................... .............. ...... 453 9. Sense Organs ................................................................................ 453

10. Mitotic Activity ........................................................................... 454 11. Behavioral Changes ...................................................................... 455 12. Median Eminence ........................................................................ 457 13. Conclusion ....... ...... ... ..... ... ..... ... ....... ........ .............. ..... ....... .......... 457 References ........................................................................................... 458

CONTENTS

Chapter 14 Changes in the Blood during Amphibian Metamorphosis Robert H. Broyles

xix

1. Introduction ................................................................................. 461 2. An Overview of Changes in Serum Proteins and Iron

Metabolism .................................................................................. 463 2.1. Changes in Blood Osmolarity, Serum Protein

Concentration, and Serum Albumin ........ ................ ........ 463 2.2. Changes in the Circulating Levels of Thyroid Hormones

and Binding Proteins ......................................................... 464 2.3. Changes in Iron Transport, Metabolism, and Storage ..... 465

3. Changes in the Hemoglobins and Red Blood Cells ................... 467 3.1. Changes in Hb Structure and Function ............................ 467 3.2. Developmental Timing of the Hb Transition in Various

Amphibians ........................................................................ 470 3.3. Changes in Morphology and in Other Properties of the

RBCs ................................................................................... 472 4. Central Questions Pertaining to the RBC-Hb Transition in

Bullfrogs ........................................................................................ 474 4.1. Do Adult and Larval Hbs Share Any Globin Chains? ..... 474 4.2. Are Adult and Larval Hbs Contained in the Same RBCs

during Metamorphosis? ..................................................... 475 4.3. Is the RBC-Hb Transition Mediated by a Change in

Erythropoietic Sites? .......................................................... 478 4.4. Does the Life Span of RBCs Change during

Metamorphosis? ................................................................. 481 4.5. Do Thyroid Hormones Have a Direct Effect on the Switch

from Larval to Adult Globin Gene Expression? .............. 482 4.6. What Is the Origin of the Stem Cells That Give Rise to

Larval and Adult RBCs? .................................................... 485 5. Summary ...................................................................................... 485

References ........................................................................................... 489

Chapter 15

Biochemical Character,ization of Organ Differentiation and Maturation

Sandra r. Smith-Gill and Virginia Carver

1. Introduction ................................................................................. 491 2. The Liver ........................ ........................... ................................... 492

2.1. DNA Synthesis, Cell Division, and Nuclear Morphology ........................................................................ 492

xx CONTENTS

2.2. Protein Synthesis, RNA Metabolism, and Cytoplasmic Morphology during Metamorphosis ................................. 500

2.3. Liver Glycogen ............................ ..... .................................. 506 2.4. Mitochondrial Structure and Function during

Metamorphosis .................................................................. 507 2.5. Temperature Effects on Liver Metamorphosis ................ 509 2.6. Summary ............................................................................ 511

3. The Kidney ................................................................................... 512 4. The Intestine ...................................................... .......................... 513

4.1. Loss of Primary Epithelium and Shortening of the Gut 514 4.2. Proliferation of Secondary Epithelium and Development

of Extraepithelial Tissues .................................................. 516 4.3. Summary ............................................................................ 517

5. The Integument ........................................................................... 518 5.1. The Pigmentary System .................................................... 518 5.2. Nonpigmentary Changes ................................................... 530

6. The Eye ......................................................................................... 533 6.1. The Lens ................................ .............. ................ ............... 534 6.2. The Retina ................................ ................... ....................... 535

7. Summary and Conclusions ......................................................... 540 References ........................................................................ ................... 542

Chapter 16

The Dual Role of Thyroid Hormones in Vertebrate Development and Calorigenesis Earl Frieden

1. Introduction .... ................................................................. ............ 545 2. The Role of Iodine in Invertebrates ............................................ 547

2.1. The Mystique of Iodine ..................................................... 548 3. Thyroid Hormone Dose-Response Relationships ..................... 550 4. Thyroid Hormone Receptors ...... ............ .............. ............ ........... 552 5. Thyroid Hormone Effects in Poikilothermic Vertebrates ......... 552 6. Metamorphic Hormones in Amphibians .... .............. ............ ...... 553 7. Thyroid Hormone Action in Birds .............................................. 555 8. Metabolism and Calorigenesis .................................................... 556

8.1. Hypo- and Hyperthyroidism ............................................. 557 9. Thyroid Hormones and Differentiation ..................................... 557

10. Mechanism of Action of Thyroid Hormones .......... .............. ..... 560 10.1. Control of Nuclear Transcription and Protein Synthesis 561 10.2. Alternative Mechanisms of Thyroid Hormone Action ... 562

References ........................................................................................... 563

Index .................................................................................................... 565